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Comparative analysis of phenolic profiles of ovipositional fluid of Rhinusa pilosa (Mecinini, Curculionidae) and its host plant Linaria vulgaris (Plantaginaceae)

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Abstract

Rhinusa pilosa (Gyllenhal) is a highly specific weevil that induces stem galls on the common toadflax Linaria vulgaris Mill. females oviposit the eggs near the apex of a growing shoot. The act of oviposition is accompanied by secretion of an ovipositional fluid, which is considered to be cecidogen, directly involved in gall induction. The remains of cecidogenic fluid were collected from the surface of the oviposition point on the stem. We performed a comparative analysis of the phenolics extracted from cecidogen, the stem and galls of L. vulgaris and adult and larva of R. pilosa by HPLC-DAD. One compound with A max at 273, 332 nm (R t 30.65 min) was exclusively found in the methanol extract of cecidogen. To further characterize the cecidogen and stem phenolic profiles, we used UHPLC coupled with an OrbiTrap mass analyzer. Among 49 phenolic compounds extracted from both the ovipositional fluid and the plant, protocatechuic acid and two phenolic glycosides were exclusively found in cecidogen: diosmetin-O-acetylrutinoside and an unidentified compound. The unknown compound produced an MS2 base peak at 387 and 327 and 267 m/z base peaks at MS3 and MS4 fragmentation, respectively, and had the molecular formula C32H31O18. The plausible role of phenolic compounds in the induction of gall formation on L. vulgaris is discussed.

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References

  • Abrahamson WG, Weis AE (1987) Nutritional ecology of arthropod gallmakers. In: Slanskyand FJ, Rodriquez G (eds) Nutritional ecology of insects, mites, spiders, and related invertebrates. Wiley, New York, pp 235–258

    Google Scholar 

  • Ahmed S, Brattsten LB (2013) Molecular aspects of insect-plant associations. Springer, Berlin

    Google Scholar 

  • Barbehenn RV, Constabel CP (2011) Tannins in plant–herbivore interactions. Phytochemistry 72(13):1551–1565. doi:10.1016/j.phytochem.2011.01.040

    Article  CAS  PubMed  Google Scholar 

  • Barnewall EC (2011) Plant-insect interactions between yellow toadflax, Linaria vulgaris, and a potential biocontrol agent, the gall-forming weevil, Rhinusa pilosa. Doctoral dissertation, University of Lethbridge, Department of Biological Sciences

  • Barnewall EC, De Clerck-Floate RA (2012) A preliminary histological investigation of gall induction in an unconventional galling system. Arthropod-Plant Int 6(3):449–459. doi:10.1007/s11829-012-9193-4

    Article  Google Scholar 

  • Bi JL, Felton GW (1995) Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J Chem Ecol 21(10):1511–1530. doi:10.1007/BF02035149

    Article  CAS  PubMed  Google Scholar 

  • Byers JA, Brewer JW, Denna DW (1976) Plant growth hormones in pinyon insect galls. Marcellia 39:125–134. http://www.chemical-ecology.net/papers/mar76.htm

  • Caldara R, Desancic M, Gassmann A, Legarreta L, Emerson BC, Toševski I (2008) On the identity of Rhinusa hispida (Brullé) and its current synonyms (Coleoptera: Curculionidae). Zootaxa 1805:61–68

    Google Scholar 

  • Cheriet T, Mancini I, Seghiri R, Benayache F, Benayache S (2015) Chemical constituents and biological activities of the genus Linaria (Scrophulariaceae). Nat Prod Res. doi:10.1080/14786419.2014.999243

    PubMed  Google Scholar 

  • Coruh S, Ercisli S (2010) Interactions between galling insects and plant total phenolic contents in Rosa canina L. genotypes. Sci Res Essays 5(14):1935–1937

    Google Scholar 

  • Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7(7):1085. doi:10.1105/tpc.7.7.1085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dreger-Jauffret F, Shorthouse JD (1992) Diversity of gall-inducing insects and their galls. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, New York, pp 8–33

    Google Scholar 

  • Gassmann A, De Clerck-Floate R, Sing S, Toševski I, Mitrović M, Krstić O (2014) Biology and host specificity of Rhinusa pilosa, a recommended biological control agent of Linaria vulgaris. Biocontrol 59(4):473–483. doi:10.1007/s10526-014-9578-7

    Article  Google Scholar 

  • Gupta JP (2011) Morphometric dynamics and growth differentiation in midvein and petiole galls of Salvodora oleoides Dine (Salvadoraceae). Phytomorphology 61(1/2):28–35

    Google Scholar 

  • Hua H, Li X, Xing S, Pei Y (2004) Study on the chemical constituents of Linaria vulgaris. Zhongguoyaoxuezazhi (Zhongguoyaoxuehui: 1989) 40(9):653–656

    Google Scholar 

  • Kjellberg F, Jousselin E, Hossaert-McKey M, Rasplus JY (2005) Biology, ecology, and evolution of fig-pollinating wasps (Chalcidoidea, Agaonidae). In: Raman A, Schaefer CW, Withers TM (eds) Biology, ecology, and evolution of gall-inducing arthropods. Sciences Publishers, Enfield, pp 539–572

    Google Scholar 

  • Lalonde RG, Shorthouse JD (1984) Developmental morphology of the gall of Urophora cardui (Diptera, Tephritidae) in the stems of Canada thistle (Cirsiumarvense). Can J Bot. doi:10.1139/b98-143

    Google Scholar 

  • Leggo JJ, Shorthouse JD (2006) Development of stem galls induced by Diplolepistriforma (Hymenoptera: Cynipidae) on Rosa acicularis (Rosaceae). Can Entomol 138:661–680. doi:10.4039/N05-086

    Article  Google Scholar 

  • Lewis IF, Walton L (1947) Initiation of the cone gall of witch hazel. Science 106(2757):419–420. doi:10.1126/science.106.2757.419

    Article  CAS  PubMed  Google Scholar 

  • Mandal SM, Chakraborty D, Dey S (2010) Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signal Behav 5(4):359–368. doi:10.4161/psb.5.4.10871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mani MS (1964) Ecology of plant galls. Dr. W. Junk Publishers, The Hague

    Book  Google Scholar 

  • Mapes CC, Davies PJ (2001) Indole-3-acetic acid and ball gall development on Solidago altissima. New Phytol 151(1):195–202. doi:10.1046/j.1469-8137.2001.00161.x

    Article  CAS  Google Scholar 

  • Morgan ED (2004) Biosynthesis in insects. Royal Society of Chemistry, London

    Google Scholar 

  • Motta LB, Kraus JE, Salatino A, Salatino MLF (2005) Distribution of metabolites in galled and non-galled foliar tissues of Tibouchina pulchra. Biochem Syst Ecol 33:971–981. doi:10.1016/j.bse.2005.02.004

    Article  CAS  Google Scholar 

  • Nyman T, Julkunen-Tiitto R (2000) Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proc Natl Acad Sci 97(24):13184–13187. doi:10.1073/pnas.230294097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Otsuka H (1992) Isolation of isolinariins A and B, new flavonoid glycosides from Linaria japonica. J Nat Prod 55(9):1252–1255. doi:10.1021/np50087a011

    Article  CAS  Google Scholar 

  • Raman A (2011) Morphogenesis of insect-induced plant galls: facts and questions. Flora 206(6):517–533. doi:10.1016/j.flora.2010.08.004

    Article  Google Scholar 

  • Rani PU, Jyothsna Y (2010) Biochemical and enzymatic changes in rice plants as a mechanism of defense. Acta Physiol Plant 32(4):695–701. doi:10.1007/s11738-009-0449-2

    Article  CAS  Google Scholar 

  • Rey LA (1992) Developmental morphology of two types of Hymenopterous galls. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, New York, pp 87–101

    Google Scholar 

  • Saniewski M, Ueda J, Miyamoto K (2002) Relationships between jasmonates and auxin in regulation of some physiological processes in higher plants. Acta Physiol Plant 24(2):211–220. doi:10.1007/s11738-002-0013-9

    Article  CAS  Google Scholar 

  • Shorthouse JD, Rohfritsch O (1992) Biology of insect-induced galls. Oxford University Press, Oxford

    Google Scholar 

  • Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends Eco Evol 18(10):512–522. doi:10.1016/S0169-5347(03)00247-7

    Article  Google Scholar 

  • Sun Q, Chang L, Ren Y, Cao L, Sun Y, Du Y, Shi X, Wang Q, Zhang L (2012) Simultaneous analysis of 11 main active components in Cirsium setosum based on HPLC-ESI-MS/MS and combined with statistical methods. J Sep Sci 35(21):2897–2907. doi:10.1002/jssc.201200359

    Article  CAS  PubMed  Google Scholar 

  • Tamagnone L, Merida A, Stacey N, Plaskitt K, Parr A, Chang CF et al (1998) Inhibition of phenolic acid metabolism results in precocious cell death and altered cell morphology in leaves of transgenic tobacco plants. Plant Cell 10(11):1801–1816. doi:10.2307/3870905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toševski I, Caldara R, Jović J, Hernández-Vera G, Baviera C, Gassmann A, Emerson BC (2015) Host-associated genetic divergence and taxonomy in the Rhinusa pilosa Gyllenhal species complex: an integrative approach. Syst Entomol 40(1):268–287. doi:10.1111/syen.12109

    Article  Google Scholar 

  • Treutter D (2006) Significance of flavonoids in plant resistance: a review. Environ Chem Lett 4(3):147–157. doi:10.1007/s10311-006-0068-8

    Article  CAS  Google Scholar 

  • Valdés B (1970) Flavonoid pigments in flower and leaf of the genus Linaria (Scrophulariaceae). Phytochemistry 9(6):1253–1260. doi:10.1016/s0031-9422(00)85316-9

    Article  Google Scholar 

  • Vereecke D, Messens E, Klarskov K, De Bruyn A, Van Montagu M, Goethals K (1997) Patterns of phenolic compounds in leafy galls of tobacco. Planta 201(3):342–348. doi:10.1007/s004250050076

    Article  CAS  PubMed  Google Scholar 

  • Vidović M, Morina F, Milić S, Zechmann B, Albert A, Winkler JB, Veljović Jovanović S (2015) Ultraviolet-B component of sunlight stimulates photosynthesis and flavonoid accumulation in variegated Plectranthus coleoides leaves depending on background light. Plant Cell Environ 38(5):968–979. doi:10.1111/pce.12471

    Article  PubMed  Google Scholar 

  • Vrchovská V, Spilková J, Valentão P, Sousa C, Andrade PB, Seabra RM (2008) Assessing the antioxidative properties and chemical composition of Linaria vulgaris infusion. Nat Prod Res 22(9):735–746. doi:10.1080/14786410601132360

    Article  PubMed  Google Scholar 

  • War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7(10):1306–1320. doi:10.4161/psb.21663

    Article  PubMed  PubMed Central  Google Scholar 

  • Weis AE, Abrahamson WG (1986) Evolution of host-plant manipulation by gall makers: ecological and genetic factors in the Solidago-Eurosta system. Am Nat. doi:10.1086/284513

    Google Scholar 

Download references

Acknowledgments

This research was supported by III43001, III43010 and OI172017 project funded by the Ministry of Education, Science and Technological Development of the Republic of Serbia. The authors would like to thank Prof. Umeo Takahama, Department of Health and Nutrition Care, University of East Asia, Japan, for useful suggestions and comments during the preparation of the manuscript.

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Authors and Affiliations

  1. Institute for Multidisciplinary Research, University of Belgrade, Belgrade, Serbia

    Ana Sedlarević, Filis Morina & Sonja Veljović-Jovanović

  2. CABI, Delémont, Switzerland

    Ivo Toševski

  3. Faculty of Chemistry, University of Belgrade, Belgrade, Serbia

    Uroš Gašić & Maja Natić

  4. Department of Plant Pests, Institute for Plant Protection and Environment, Zemun, Serbia

    Ivo Toševski, Jelena Jović & Oliver Krstić

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  1. Ana Sedlarević
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Correspondence to Filis Morina.

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Handling Editor: Anna-Karin Borg-Karlson.

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Sedlarević, A., Morina, F., Toševski, I. et al. Comparative analysis of phenolic profiles of ovipositional fluid of Rhinusa pilosa (Mecinini, Curculionidae) and its host plant Linaria vulgaris (Plantaginaceae). Arthropod-Plant Interactions 10, 311–322 (2016). https://doi.org/10.1007/s11829-016-9435-y

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